Arabidopsis plants perform arithmetic division to prevent starvation at night

Photosynthetic starch reserves that accumulate in Arabidopsis leaves during the day decrease approximately linearly with time at night to support metabolism and growth. We find that the rate of decrease is adjusted to accommodate variation in the time of onset of darkness and starch content, such that reserves last almost precisely until dawn. Generation of these dynamics therefore requires an arithmetic division computation between the starch content and expected time to dawn. We introduce two novel chemical kinetic models capable of implementing analog arithmetic division. Predictions from the models are successfully tested in plants perturbed by a night-time light period or by mutations in starch degradation pathways. Our experiments indicate which components of the starch degradation apparatus may be important for appropriate arithmetic division. Our results are potentially relevant for any biological system dependent on a food reserve for survival over a predictable time period. DOI: http://dx.doi.org/10.7554/eLife.00669.001

[1]  M. Steup,et al.  Phosphorylation of C6‐ and C3‐positions of glucosyl residues in starch is catalysed by distinct dikinases , 2006, FEBS letters.

[2]  David Thorneycroft,et al.  Diurnal Changes in the Transcriptome Encoding Enzymes of Starch Metabolism Provide Evidence for Both Transcriptional and Posttranscriptional Regulation of Starch Metabolism in Arabidopsis Leaves1 , 2004, Plant Physiology.

[3]  Mark Stitt,et al.  Circadian control of root elongation and C partitioning in Arabidopsis thaliana. , 2011, Plant, cell & environment.

[4]  Peter A. J. Hilbers,et al.  Computing Algebraic Functions with Biochemical Reaction Networks , 2009, Artificial Life.

[5]  Alison M. Smith,et al.  Control of Starch Granule Numbers in Arabidopsis Chloroplasts1[W][OA] , 2011, Plant Physiology.

[6]  Y. Benenson.  Biomolecular computing systems: principles, progress and potential , 2012, Nature Reviews Genetics.

[7]  T. Sharkey,et al.  Daylength and Circadian Effects on Starch Degradation and Maltose Metabolism1 , 2005, Plant Physiology.

[8]  Yves Gibon,et al.  Global Transcript Levels Respond to Small Changes of the Carbon Status during Progressive Exhaustion of Carbohydrates in Arabidopsis Rosettes1[W][OA] , 2008, Plant Physiology.

[9]  W. Haworth,et al.  Starch , 1940, Springer Japan.

[10]  T. Rees,et al.  Turnover of starch and sucrose in roots of Pisum sativum , 1988 .

[11]  D. Thorneycroft,et al.  α-Amylase Is Not Required for Breakdown of Transitory Starch in Arabidopsis Leaves* , 2005, Journal of Biological Chemistry.

[12]  Ted M. Lakowski,et al.  Analytical Biochemistry , 1960, Nature.

[13]  P. Geigenberger,et al.  Identification of a Novel Enzyme Required for Starch Metabolism in Arabidopsis Leaves. The Phosphoglucan, Water Dikinase1[w] , 2005, Plant Physiology.

[14]  H. Sauro,et al.  Preliminary Studies on the In Silico Evolution of Biochemical Networks , 2004, Chembiochem : a European journal of chemical biology.

[15]  D. Bray.  Protein molecules as computational elements in living cells , 1995, Nature.

[16]  Alison M. Smith,et al.  Starch and the clock: the dark side of plant productivity. , 2011, Trends in plant science.

[17]  J. Fisahn,et al.  Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. , 2004, The Plant journal : for cell and molecular biology.

[18]  H. Petty,et al.  An enzymatic fluorimetric assay for glucose-6-phosphate: application in an in vitro Warburg-like effect. , 2009, Analytical biochemistry.

[19]  Steve A. Kay,et al.  Reciprocal Regulation Between TOC1 and LHY/CCA1 Within the Arabidopsis Circadian Clock , 2001, Science.

[20]  A. Blennow,et al.  A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[21]  M. Stitt,et al.  Starch turnover: pathways, regulation and role in growth. , 2012, Current opinion in plant biology.

[22]  Alison M. Smith.  Starch in the Arabidopsis plant , 2012 .

[23]  J. Robin,et al.  Long-term fasting and re-feeding in penguins. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[24]  G. Visser,et al.  Body condition of shorebirds upon arrival at their Siberian breeding grounds , 2009, Polar Biology.

[25]  Robert E. Marra,et al.  Frontiers of Plant Science , 2005 .

[26]  A. Satake,et al.  Dynamical feedback between circadian clock and sucrose availability explains adaptive response of starch metabolism to various photoperiods , 2013, Front. Plant Sci..

[27]  D. MacLean,et al.  A Putative Phosphatase, LSF1, Is Required for Normal Starch Turnover in Arabidopsis Leaves1[W][OA] , 2009, Plant Physiology.

[28]  Wendell A Lim,et al.  Design principles of regulatory networks: searching for the molecular algorithms of the cell. , 2013, Molecular cell.

[29]  M. Stitt,et al.  Coordination of carbon supply and plant growth. , 2007, Plant, cell & environment.

[30]  Theodore J. Perkins,et al.  Implementing Arithmetic and Other Analytic Operations By Transcriptional Regulation , 2008, PLoS Comput. Biol..

[31]  M. Steup,et al.  Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. , 2000, The Plant journal : for cell and molecular biology.

[32]  M. Steup,et al.  The Two Plastidial Starch-Related Dikinases Sequentially Phosphorylate Glucosyl Residues at the Surface of Both the A- and B-Type Allomorphs of Crystallized Maltodextrins But the Mode of Action Differs1 , 2009, Plant Physiology.

[33]  Mark Stitt,et al.  Circadian control of carbohydrate availability for growth in Arabidopsis plants at night , 2010, Proceedings of the National Academy of Sciences.